T-cell receptor-induced NF-kappaB activation is negatively regulated by E3 ubiquitin ligase Cbl-b

Mol Cell Biol. 2008 Apr;28(7):2470-80. doi: 10.1128/MCB.01505-07. Epub 2008 Jan 28.

Abstract

It has previously been shown that E3 ubiquitin ligase Casitas B-lineage lymphoma-b (Cbl-b) negatively regulates T-cell activation, but the molecular mechanism(s) underlying this inhibition is not completely defined. In this study, we report that the loss of Cbl-b selectively results in aberrant activation of NF-kappaB upon T-cell antigen receptor (TCR) ligation, which is mediated by phosphatidylinositol 3-kinase (PI3-K)/Akt and protein kinase C-theta (PKC-theta). TCR-induced hyperactivation of Akt in the absence of Cbl-b may potentiate the formation of caspase recruitment domain-containing membrane-associated guanylate kinase protein 1 (CARMA1)-B-cell lymphoma/leukemia 10 (Bcl10)-mucosa-associated lymphatic tissue 1(MALT1) (CBM) complex, which appears to be independent of PKC-theta. Cbl-b associates with PKC-theta upon TCR stimulation and regulates TCR-induced PKC-theta activation via Vav-1, which couples PKC-theta to PI3-K and allows it to be phosphorylated. PKC-theta then couples IkappaB kinases (IKKs) to the CBM complex, resulting in the activation of the IKK complex. Therefore, our data provide the first evidence to demonstrate that the down-regulation of TCR-induced NF-kappaB activation by Cbl-b is mediated coordinately by both Akt-dependent and PKC-theta-dependent signaling pathways in primary T cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / deficiency
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Adaptor Proteins, Signal Transducing / physiology*
  • Animals
  • Apoptosis Regulatory Proteins / deficiency
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • B-Cell CLL-Lymphoma 10 Protein
  • CARD Signaling Adaptor Proteins / deficiency
  • CARD Signaling Adaptor Proteins / genetics
  • CARD Signaling Adaptor Proteins / metabolism
  • CD28 Antigens / physiology
  • Enzyme Activation
  • I-kappa B Kinase / metabolism
  • Isoenzymes / deficiency
  • Isoenzymes / genetics
  • Isoenzymes / physiology*
  • Lymphocyte Activation / physiology*
  • Membrane Microdomains / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Multiprotein Complexes
  • NF-kappa B / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Kinase C / deficiency
  • Protein Kinase C / genetics
  • Protein Kinase C / physiology*
  • Protein Kinase C-theta
  • Proto-Oncogene Proteins c-akt / physiology*
  • Proto-Oncogene Proteins c-cbl / deficiency
  • Proto-Oncogene Proteins c-cbl / genetics
  • Proto-Oncogene Proteins c-cbl / physiology*
  • Proto-Oncogene Proteins c-vav / deficiency
  • Proto-Oncogene Proteins c-vav / genetics
  • Proto-Oncogene Proteins c-vav / physiology*
  • Receptors, Antigen, T-Cell / physiology*
  • Signal Transduction / physiology
  • T-Lymphocytes / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • B-Cell CLL-Lymphoma 10 Protein
  • Bcl10 protein, mouse
  • CARD Signaling Adaptor Proteins
  • CD28 Antigens
  • Card11 protein, mouse
  • Cblb protein, mouse
  • Isoenzymes
  • Multiprotein Complexes
  • NF-kappa B
  • Proto-Oncogene Proteins c-vav
  • Receptors, Antigen, T-Cell
  • Vav1 protein, mouse
  • Proto-Oncogene Proteins c-cbl
  • Phosphatidylinositol 3-Kinases
  • Akt1 protein, mouse
  • Proto-Oncogene Proteins c-akt
  • I-kappa B Kinase
  • Prkcq protein, mouse
  • Protein Kinase C
  • Protein Kinase C-theta